GBE

Horizontal Gene Transfer Contributes to the Evolution of Herbivory

Nicky Wybouw,*,1 Yannick Pauchet,2 David G. Heckel,2 and Thomas Van Leeuwen*,1,3 1Department of Evolutionary Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, the Netherlands 2Department of Entomology, Max Planck Institute for Chemical Ecology, Jena, Germany 3Laboratory of Agrozoology, Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Gent, Belgium

*Corresponding author: E-mail: [email protected]; [email protected]. Accepted: May 9, 2016

Abstract Downloaded from Within , evolutionary transition toward herbivory is severely limited by the hostile characteristics of plants. have nonetheless counteracted many nutritional and defensive barriers imposed by plants and are currently considered as the most successful herbivores in terrestrial ecosystems. We gather a body of evidence showing that genomes of various plant feeding

and mites possess genes whose presence can only be explained by horizontal gene transfer (HGT). HGT is the asexual http://gbe.oxfordjournals.org/ transmission of genetic information between reproductively isolated species. Although HGT is known to have great adaptive signif- icance in prokaryotes, its impact on eukaryotic evolution remains obscure. Here, we show that laterally transferred genes into arthropods underpin many adaptations to phytophagy, including efficient assimilation and detoxification of plant produced metab- olites. Horizontally acquired genes and the traits they encode often functionally diversify within arthropod recipients, enabling the colonization of more host plant species and organs. We demonstrate that HGT can drive metazoan evolution by uncovering its prominent role in the adaptations of arthropods to exploit plants. Key words: arthropods, horizontal gene transfer, herbivory. by guest on September 24, 2016

Introduction cuticles and/or by the production of chemical defenses Plants have evolved a wide and complex set of adaptations to (Howe and Jander 2008). Defensive phytochemicals, or survive the many stressors present in their environment. These plant allelochemicals, can repulse and poison herbivores or include abiotic factors such as drought and nutrition-poor interfere with the assimilation of plant nutrients inside the soils, but also herbivore and pathogen attacks. During their herbivore’s gut (Whittaker and Feeny 1971). evolution, plants have transformed themselves to such a re- Nevertheless, arthropods can overcome these nutritional calcitrant and unfavorable food source that herbivory (or feed- and defensive barriers and various lineages have successfully ing exclusively on plant material) has only evolved in roughly adapted to a phytophagous lifestyle. The arthropod phylum is one third of all animal species (Strong et al. 1984). Both the now considered to harbor the most successful animal herbi- nutritional and defensive qualities of plants are known to limit vores in terrestrial ecosystems, both in terms of biomass and the evolution of animal herbivory (Awmack and Leather species diversity (Strong et al. 1984; Labandeira 2002, 2006; 2002). As many plant species and tissues are characterized Schoonhoven et al. 2006)(fig. 1). Within arthropod–plant in- by a relatively high carbohydrate content, but low protein teractions, there has been an evolutionary trend for phytoph- and vitamin levels (Mattson 1980; Strong et al. 1984; agous arthropods to further specialize to a specific plant family Awmack and Leather 2002), herbivorous animals need to op- or even species by optimizing the assimilation and detoxifica- timize the assimilation of the limited supply of nutrients in tion processes (Bernays and Graham, 1988; Schoonhoven plant tissues. In addition, plants have evolved multi-layered et al. 2006). Using next-generation sequencing-based meth- defense strategies that negatively affect the reproductive per- ods, many studies are currently investigating the genomic and formance of herbivores. Plant resistance to herbivory can be genetic innovations that are associated with these evolution- achieved by physical barriers such as trichomes and waxy ary transitions to arthropod herbivory and further host plant

ß The Author 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected]

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FIG.1.—Arthropod phylogenetic tree showing documented HGT events in phytophagous chelicerate and hexapod lineages. The names of the clades harboring herbivores are depicted in green. Horizontally transferred genes coding for traits involved in plant cell wall digestion, intracellular plant metabolite assimilation, and overcoming plant defenses are depicted in blue, green, and red lines, respectively. Detailed lists of the methodologies that identified the HGT events, the nature of the horizontally transferred genes and donor and recipient species can be found in table 1. by guest on September 24, 2016 specializations. Of the identified arthropod genes that code element can be stably introduced in an animal genome, it for enzymes with a clear selective advantage to the phytoph- has to enter the nucleus within the isolated germ cell line, agous lifestyle, a subset has been identified with two unusual and needs to be adjusted to the transcription machinery of properties: high similarity to microbial genes, and absence in the recipient species. Despite these evolutionary barriers, an the majority of other lineages within the Arthropoda phylum. increasing number of apparently horizontally transferred This unusual phylogenetic distribution has often prompted the genes are being reported in arthropod herbivores. conclusion that these functional genes were introduced to the Moreover, many of these unique genes, while still coding arthropod genome by the process of horizontal gene transfer for functionally active enzymes after the HGT event, addition- (HGT), defined as the nonsexual transmission of genetic ma- ally show signs of functional diversification. Here, we discuss terial across species boundaries (Kidwell 1993; Li and Graur the different criteria that are used to establish that arthropod 1991). This entails that in contrast to the classical evolutionary herbivores are the recipients of functional foreign genetic in- model where new genes arise by duplication of pre-existing formation. We furthermore argue for an evolutionary trend in ancestral genes followed by mutation and then gradual selec- arthropods where HGT facilitates adapting to the nutritive and tion for novel functions, HGT suddenly introduces new genes defensive barriers of plants, and we argue that HGT has that had already been subjected to natural selection in a played a substantial role in the ecological success of arthropod nonrelated species. Such inferences of HGT in animal ge- herbivory within several lineages. nomes are often met with high skepticism, as the mechanisms of HGT are only well documented within the prokaryotic Detecting HGT by Its domain of life. HGT is accepted to be widespread and preva- lent among prokaryotes and acknowledged as a major force Phylogenetic Signatures in their adaptive evolution (Koonin et al. 2001; Springael and The direct observation of an individual HGT event that oc- Top 2004; Pal et al. 2005). An additional argument against curred in the distant past is physically impossible. Therefore, HGT in animal genomes is that eukaryotic biology presents too putative HGT events must be inferred from currently available many barriers to HGT. Before a mobile functional genetic data, and the hypothesis that a specific HGT event has

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occurred can only be tested by probabilistic methods. As HGT Doubts about the identification of an HGT event by phylo- presents an unusually high degree of sequence similarity be- genetics often arise due to a misunderstanding of the ances- tween the distantly related donor and recipient species for the tral distribution of the gene of interest. To address this gene of interest, studies employ methodologies that analyze problem, it is useful to divide phylogenetic reconstructions different properties of the nucleotide and/or amino acid se- into three major scenarios, based on the occurrence of the quence to test the HGT hypothesis. gene of interest across all lineages of the tree of life. First, HGT Molecular phylogenetics is the study of the evolutionary can convey a completely novel gene to arthropods which is history and relationships of genes across organisms by using normally absent in their entire phylogenetic lineage (fig. 2B, molecular data such as nucleotide and amino acid sequences. left tree). Here, the simple presence of the gene in an arthro- A phylogenetic analysis generates a phylogenetic tree which is pod genome already strongly favors HGT, and HGT cannot be characterized by a certain branching pattern or topology. This ruled out even if the donor clade cannot be identified by topology mirrors the courses of inheritance of the genes of suboptimal phylogenetic support. Clear-cut examples of com- interest over evolutionary time. The reliability of these topolo- pletely novel genes in plant feeding arthropods include genes gies can be inferred by various computational techniques that that code for carotenoid cyclases/synthases, chorismate estimate the confidence level of each internal bifurcation. By mutase (CM), and cyanase (Grbic et al. 2011; Novakova and Downloaded from creating a consensus tree of numerous individual gene trees Moran 2012; Wybouw et al. 2012; Sloan et al. 2014). In the (often on a genome-wide level), a species tree can be pro- second scenario, the arthropod species already harbors a re- duced where the actual speciation events are mapped. lated homologue to the potential laterally transferred Molecular phylogenetic methods are the gold standard in ar- gene (fig. 2B, middle tree). Here, HGT is inferred when the thropod studies and suggest an HGT when the gene of inter- candidate transferred and the other paralogue(s) show http://gbe.oxfordjournals.org/ est is grouped with homologues of nonrelated species by strongly divergent evolutionary histories. mites of the strongly statistically supported branches (for instance with at Tetranychidae family (Arthropoda: ) and lepidop- least 60% bootstrap support) (Efron et al. 1996)(fig. 2). In terans (Arthropoda: Hexapoda) possess a universal arthropod order to be reliable, these phylogenetic incongruence meth- cystathionine b-synthase (CBS)geneandauniquecysteine ods require: (1) a well-established species phylogeny which is synthase (or b-cyanoalanine synthase) (CAS) gene, part of needed as a reference topology and (2) an expansive set of the same b-substituted alanine synthase gene family, but closely and step-wise more distantly related homologous with the latter normally restricted to bacterial and plant spe- genes in order to avoid sampling bias. For many arthropod

cies. Wybouw et al. (2014) showed phylogenetically that the by guest on September 24, 2016 studies, both requirements can be met as a significant part of mite and lepidopteran CAS enzymes clustered together with the arthropod phylogenomic tree is well mapped and keeps bacterial and plant enzymes, while their CBS enzymes were improving due to the increasing number of sequenced arthro- embedded with high probability in a eukaryotic group of en- pod genomes and transcriptomes (Regier et al. 2010; Wheat zymes. In a third scenario (fig. 2 B, right tree), the close ances- and Wahlberg 2013; Misofetal.2014). These genomic se- tral homologue to the transmitted gene is lost in the recipient quences simultaneously offer an unbiased set of orthologues species. Here, HGT is identified when the homologues of spe- spanning both short taxonomic distances (often within the cies related to the recipient exhibit distinct evolutionary histo- same ) and large ones (between different subphyla). In ries compared with the gene of interest. For instance, Ahn order to be convincing as a general methodology, phyloge- et al. (2014) suggested by a phylogenetic reconstruction netic incongruence methods must also be able to reject the that an ancestral chelicerate lost the arthropod UDP-glycosyl- HGT hypothesis under appropriate conditions. For instance, transferase (UGT) gene(s) and that tetranychid mites later using this extensive sequence dataset, phylogenetic analysis horizontally received novel UGTs, clearly different from the ver- finally concluded that a much-debated putative horizontally tically transmitted arthropod UGT sequences. Independent of transferred gene in termites is instead much more likely to be a the ancestral distribution, as gene duplications, differential typical vertically transmitted gene, present in various other gene losses and evolutionary convergence can also result in arthropod lineages (Lo et al. 2011). A potential shortcoming a phylogenetic reconstruction where distant species lineages of this type of test is that the putative horizontally transferred cluster together, the likelihood of an HGT event versus alter- gene and the set of available homologues may not contain a native scenarios should always be weighed (Ku et al. 2015). strong enough phylogenetic signal (for instance due to short sequence lengths). Alignments of such sequence sets typically Detecting HGT by Other lead to various poorly supported branches in phylogenetic re- constructions. When faced with nonoptimal tree support Probabilistic Methods values at critical bipartitions, studies often combine multiple To maximize the likelihood of correctly identifying an HGT phylogenetic methods to minimize the chances of an errone- event, studies can incorporate additional, independent prob- ous identification of an HGT event in arthropods (Wybouw abilistic methods before concluding that a gene arose by HGT. et al. 2012; Husnik et al. 2013; Pauchet and Heckel 2013). Many of these approaches take advantage of the high

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A

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FIG.2.—(A) Left: A species tree where the bifurcations represent speciation events. Species trees are based on the sequence information of multiple by guest on September 24, 2016 genes (often genome-wide; phylogenomic trees) and depict how species are related. Here, horizontal transfer of a single gene is not expected to changethe phylogenomic tree. Right: the three known mechanisms of HGT in prokaryotes; transformation (direct uptake of foreign DNA), conjugation (plasmid- mediated uptake) and transduction (virus-mediated uptake). (B) Phylogenetic analysis of a gene of interest can detect an HGT event by showing that a particular species is embedded within a group of distantly related organisms. The implanted species and the surrounding clade are then considered to be the recipient species and donor clade of the transferred gene, respectively. Three scenarios are depicted of how HGT can distort the phylogenetic reconstruction of a single gene. These scenarios are characterized by a certain ancestral gene distribution across the tree of life. Left: The gene is originally restricted to a certain phylogenetic clade, distantly related to the recipient species. As the horizontally transferred gene does not have related homologues within the clade harboring the recipient species, it is unique to the recipient. Middle: The gene is present in all lineages, but a gene copy from a distant species supplements an existing innate homologue in the recipient genome. Right: Here, a foreign gene replaces the original homologue in the recipient genome through HGT. In each case however, the possibility of alternative scenarios to an HGT event should always be considered (for instance, differential gene loss across the tree of life).

number of sequenced genomes across the tree of life. After in combination with a phylogenetic analysis as it has several phylogenetic analysis, one approach analyzes the codon con- imperfections. First, a true HGT event can be overlooked if the tent of the entire genome of the recipient and putative donor nonrelated donor and recipient species have similar genomic species. As phylogenetic reconstruction usually does not un- codon contents. Second, even if the donor and recipient ge- cover the exact donor species, the genomes of a broader nomes are characterized by distinctly different codon con- group of species are included in the codon content analysis. tents, the hypothesis of an ancient HGT can still be rejected. Based on the theory that the codon usage pattern of all Once a gene is laterally incorporated, it is subjected to the coding sequences within a certain genome is similar and same mutational processes as the rest of the recipient’s that this genomic signature varies between species genome and will, over time, homogenize its codon content (Lawrence and Ochman 1997), a horizontally transferred with its genomic surroundings, in a process called ameliora- gene candidate can be confirmed by detecting a different tion (Lawrence and Ochman 1997). Indeed, in arthropods and codon content compared with the rest of the recipient other animals, laterally acquired genes often exhibit nondis- genome. However, this methodology should always be used tinguishable codon contents from those of ancestral, innate

1788 Genome Biol. Evol. 8(6):1785–1801. doi:10.1093/gbe/evw119 Advance Access publication June 15, 2016 HGT in Arthropod Herbivores GBE

genes (Danchin et al. 2010; Wybouw et al. 2014). Therefore, For instance, after identifying potential laterally transferred this methodology only gives further support when the HGT genes coding for xylanases in a midgut transcriptome of the was very recent and when the reproductively isolated species mustard leaf (), Pauchet and have distinctly different genomic codon signatures. More and Heckel (2013) screened a genomic DNA fosmid library to more HGT cases with an arthropod recipient are being exam- prove that two laterally transferred xylanase genes reside in ined with this technique, in addition to the standard phyloge- the beetle genome and are neighbored by -derived netic analysis (Sun et al. 2013; Wybouw et al. 2014; van Ohlen transposable elements (TEs). Using next-generation sequenc- et al. 2016). ing technology, multiple genomic studies of various arthropod Using the plethora of sequenced genomes, families of lineages show that horizontally transferred genes are present orthologues can be systemically classified (Tatusov et al. on large genomic scaffolds, where they are flanked by typical 1997; Li et al. 2003). These comparative genomics techniques arthropod genes (Grbic et al. 2011; Husnik et al. 2013; Vega allow for a new approach to examine the HGT hypothesis: the et al. 2015; Zhao et al. 2015). As genome assemblies can have analysis of the phyletic pattern within a certain orthologue imperfect computational sequence filters (Baker 2012), an ap- family. The phyletic pattern is the occurrence or absence of parent lateral acquisition can be an artifact due to the pres- species within these defined clusters of orthologues. For in- ence and incorrect concatenation of contaminating bacterial Downloaded from stance, when a fungal lineage is detected within an otherwise sequences with other reads from the shotgun library exclusively bacterial protein family, an HGT event can be in- (Koutsovoulos et al. 2016). If a Bacterial Artificial ferred. This methodology has confirmed multiple HGT events Chromosome library is available, this possibility can be ruled to microorganisms (Koonin et al. 2001). After a BLASTP search out (Pauchet et al. 2014b). Potential genome assembly arti- of a proteome under investigation against a large species cu- facts can also be ruled out by validating the genomic sequence http://gbe.oxfordjournals.org/ rated sequence database, Clarke’s phylogenetic discordance through PCR amplifications which often include geographi- test identifies horizontally transferred genes that exhibit sta- cally distinct arthropod populations. After identifying a hori- tistically significantly different similarity patterns compared zontally transferred gene, encoding for a mannanase, in the with the median similarity pattern shown by the proteome genome of the coffee berry borer beetle (Hypothenemus (Clarke et al. 2002).These and other methodologies are not hampei), Acuna et al. (2012) showed that the transferred yet well established in arthropod studies but show great po- gene is incorporated at the same genomic location in H. tential for future studies, despite the fact that each technique hampei populations spanning Asia, Africa, and America. The

is not without its potential limitations (Koonin et al. 2001; genomic location of the horizontally transferred CAS gene in by guest on September 24, 2016 Ragan 2001; Lawrence and Ochman 2002). the spider mite species Tetranychus urticae was confirmed by PCR amplification and shown to be identical in strains sampled Incorporation of a Microbial Gene from different regions worldwide (Wybouw et al. 2014). If in the Arthropod Genome speciation in the recipient group occurred after the HGT event, the genomic region bracketing the laterally acquired The first nucleotide and amino acid sequences of horizontally gene can also be analyzed in all descendent species. The ge- transferred genes in plant feeding arthropods were mainly nomic region bracketing the CAS gene exhibits clear synteny uncovered by transcriptomic and proteomic studies (Pauchet between T. urticae and a closely related mite species, et al. 2008, 2009, 2010b; Kirsch et al. 2012). Although phy- Tetranychus evansi. Such approach was also followed by logenetic procedures strongly pointed toward an HGT sce- Wheeler et al. (2013), who uncovered a single, ancient hori- nario with an arthropod recipient, skeptical reviewers zontal transfer of a glycosyl hydrolase (GH) family 31 gene claimed that these genes and the enzymes they encode had from bacteria to the ancestor to all modern lepidopterans by such unusual phylogenetic distributions because they origi- demonstrating microsynteny neighboring the laterally trans- nated from associated free-living or symbiotic microorganisms ferred gene in different lepidopteran genomes. and were not part of the arthropod genome. Indeed, arthro- pods often host large bacterial communities in various organs, HGT and the Evolution of including their digestive tract (Buchner 1965; Watanabe and Tokuda 2010). Even though these genes exhibit strong se- Arthropod Herbivory quence similarity to bacterial genes, they often possess typical Recent comparative studies show a high prevalence of HGT in eukaryotic characteristics, strongly disfavoring the contamina- arthropod lineages, relative to other animal clades (Hotopp tion hypothesis and supportive of an HGT event. These gene et al. 2007; Hotopp 2011; Ramulu et al. 2012), which raises attributes include eukaryotic signal peptides, polyadenylation the question of how these genes and the traits they encode tails and spliceosomal introns (Acuna et al. 2012; Ahn et al. shape arthropod evolution. In this review, we will gather 2014; Luan et al. 2015). In addition, genomics now provide a strong indications that HGT from microbial species enhanced growing body of evidence showing that these bacterial genes the enzymatic repertoire of phytophagous arthropods, which are physically incorporated into arthropod genomes (table 1). in turn seems to have facilitated adaptations toward herbivory

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Table 1 eoeBo.Evol. Biol. Genome A List of Horizontally Transferred Genes into Plant Feeding Arthropods that Underpin Adaptations to Phytophagy Gene Name Donor Recipient (Order) Validation Reference C Digestion of plant cell wall components Cellulase/xylanase (GH5, sub2) Bacteroidetes Lamiinae (Coleoptera) ML, BI, G, F Danchin et al. (2010) and Pauchet et al. * (2014a) Mannanase (GH5, sub8) Bacillus H. hampei (Coleoptera) ML, MP, G, F Acuna et al. (2012) and Vega et al. (2015) ()18–81 o:019/b/v19AvneAcs ulcto ue1,2016 15, June publication Access Advance doi:10.1093/gbe/evw119 8(6):1785–1801. Xylanase (GH10) Streptomyces H. hampei (Coleoptera) ML, G, F Padilla-Hurtado et al. (2012) and Vega et al. (2015) Xylanase (GH11) g-Proteobacteria P. cochleariae (Coleoptera) ML, BI, NJ, G, F Pauchet and Heckel (2013) Polygalacturonase (GH28) Pezizomycotina Phytophaga (Coleoptera) ML, BI, G, F Kirsch et al. (2014), Shen et al. (1996), * and Shen et al. (2003) Ascomycota Lamiinae (Coleoptera) ML, BI, G, F Kirsch et al. (2014) and Pauchet et al. * (2014a) Mirinae (Hemiptera) ML, BI, F Celorio-Mancera et al. (2008) and Hull * et al. (2013) and Kirsch et al. (2014) Bacteroidetes Bruchinae (Coleoptera) ML, BI, G Kirsch et al. (2014) * g-Proteobacteria Verophasmatodea (Phasmatodea) ML, BI, MP, G Shelomi et al. (2014) * Cellulase (GH45) Fungi Phytophaga (Coleoptera) ML, G, F Pauchet et al. (2014a)* Pectin methylesterase (CE8) Bacteria Curculionoidea (Coleoptera) ML, BI, MP, G, F Evangelista et al. (2015), Kirsch et al. (2016), Pauchet et al. (2010a), Shen et al. (1999, 2005) Assimilation of intracellular plant metabolites Carbohydrate assimilation Glycosyl hydrolase (GH31) Enterococcus Lepidoptera (Lepidoptera) ML, BI, NJ, G Li et al. (2011), Sun et al. (2013),and Wheeler et al. (2013) b-fructofuranosidase (GH32) Bacteria Lepidoptera (Lepidoptera) ML, BI, NJ, G, F Daimon et al. (2008), Li et al. (2011), Sun * et al. (2013),andZhu et al. (2011) Bacteria A. planipennis (Coleoptera) ML, G Zhao et al. (2014) * Bacteria Curculionidae (Coleoptera) ML, G, F Keeling et al. (2013) and Pedezzi et al. * (2014) Bacteria M. destructor (Diptera) G Zhao et al. (2015) * Bacteria Tetranychidae (Trombidiformes) ML, G Bajdaetal.(2015)and Grbic et al. (2011) * Amino acid assimilation Argininosuccinate lyase Enterobacteriales B. tabaci (Hemiptera) ML, BI, G Luan et al. (2015) Carsonella Psylloidea (Hemiptera) ML, G Sloan et al. (2014) Argininosuccinate synthase Enterobacteriales B. tabaci (Hemiptera) ML, BI, G Luan et al. (2015) CM Enterobacteriales Aleyrodinae (Hemiptera) ML, BI, G Luan et al. (2015) * Bacteria Psylloidea (Hemiptera) ML, G Sloan et al. (2014) * GBE Cyanase Plants Tetranychidae (Trombidiformes) ML, G, F Bajdaetal.(2015), Grbic et al. (2011), * and Wybouw et al. (2012)

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Table 1 Continued Gene Name Donor Recipient (Order) Validation Reference C Cysteine synthase Methylobacteria Lepidoptera (Lepidoptera) ML, BI, NJ, G Li et al. (2011), Sun et al. (2013), Van * ()18–81 o:019/b/v19Adv doi:10.1093/gbe/evw119 8(6):1785–1801. Ohlen et al. (2016),andWybouw et al. (2014) Methylobacteria Tetranychidae (Trombidiformes) ML, G, F Bajda et al. (2015) and Wybouw et al. * (2014) g-Proteobacteria P. citri (Hemiptera) ML, BI, G Husnik et al. (2013) * Diaminopimelate epimerase Enterobacteriales B. tabaci (Hemiptera) ML, BI, G Luan et al. (2015) a-Proteobacteria P. citri (Hemiptera) ML, BI, G Husnik et al. (2013) Diaminopimelate decarboxylase Planctomycetes B. tabaci (Hemiptera) ML, BI, G Luan et al. (2015) a-Proteobacteria P. citri (Hemiptera) ML, BI, G Husnik et al. (2013) 4-Hydroxy-tetrahydrodipicolinate reductase Rickettsiales B. tabaci (Hemiptera) ML, BI, G Luan et al. (2015) Kynureninase L. grayi bacteria Lepidoptera (Lepidoptera) ML, BI, NJ, G, F Meng et al. (2009), Li et al. (2011), Sun et al. (2013),andZhu et al. (2011) methionine synthase Bacteria Tetranychidae (Trombidiformes) ML, G Bajda et al. (2015) and Grbic et al. (2011) N-methyltryptophan oxidase Bacteria B. mori (Lepidoptera) ML, BI, NJ, G Li et al. (2011), Sun et al. (2013),andZhu et al. (2011) Tryptophan 2-monooxygenase Proteobacteria P. citri (Hemiptera) ML, BI, G Husnik et al. (2013) * neAcs ulcto ue1,2016 15, June publication Access ance Vitamin assimilation Adenosylmethionine transaminase Bacteria Aleyrodinae (Hemiptera) ML, BI, G Luan et al. (2015) a-Proteobacteria P. citri (Hemiptera) ML, BI, G Husnik et al. (2013) Biotin synthase Rickettsiales Aleyrodinae (Hemiptera) ML, BI, G Luan et al. (2015) a-Proteobacteria P. citri (Hemiptera) ML, BI, G Husnik et al. (2013) Dethiobiotin synthase a-Proteobacteria P. citri (Hemiptera) ML, BI, G Husnik et al. (2013) GTP cyclohydrolase g-Proteobacteria P. citri (Hemiptera) ML, BI, G Husnik et al. (2013) Riboflavin synthase Bacteria Psylloidea (Hemiptera) ML, G Sloan et al. (2014) Fused deaminase/reductase a-Proteobacteria P. citri (Hemiptera) ML, BI, G Husnik et al. (2013) Carotenoid assimilation Carotenoid desaturase Mucoromycotina Aphididae (Hemiptera) ML, BI, G, F Moran and Jarvik (2010) and Novakova and Moran (2012) Adelgidae (Hemiptera) ML, BI Novakova and Moran (2012) Zygomycota Tetranychidae (Trombidiformes) ML, BI, G Altincicek et al. (2011), Bajda et al. (2015), and Grbic et al. (2011) Mucorales Cecidomyiidae (Diptera) ML, BI, G Cobbs et al. (2013) Fused carotenoid cyclase/synthase Fungi Macrosiphini (Hemiptera) ML, G Moran and Jarvik (2010) Zygomycota Tetranychidae (Trombidiformes) ML, BI, G Altincicek et al. (2012), Bajda et al. (2015), GBE and Grbic et al. (2011) Mucorales Cecidomyiidae (Diptera) ML, BI, G Cobbs et al. (2013)

1791 (continued)

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Table 1 Continued

()18–81 o:019/b/v19AvneAcs ulcto ue1,2016 15, June publication Access Advance doi:10.1093/gbe/evw119 8(6):1785–1801. Gene Name Donor Recipient (Order) Validation Reference C Overcoming plant defenses CAS Methylobacteria Lepidoptera (Lepidoptera) ML, BI, NJ, G, F Li et al. (2011), Sun et al. (2013), Van * Ohlen et al. (2016),andWybouw et al. (2014) Methylobacteria Tetranychidae (Trombidiformes) ML, G, F Bajda et al. (2015) and Wybouw et al. * (2014) g-Proteobacteria P. citri (Hemiptera) ML, BI, G Husnik et al. (2013) * CM Enterobacteriales Aleyrodinae (Hemiptera) ML, BI, G Luan et al. (2015) * Bacteria Psylloidea (Hemiptera) ML, G Sloan et al. (2014) Cyanase Plants Tetranychidae (Trombidiformes) ML, G, F Bajda et al. (2015), Grbic et al. (2011), * and Wybouw et al. (2012) b-fructofuranosidase Bacteria B. mori (Lepidoptera) ML, BI, NJ, G, F Daimon et al. (2008), Li et al. (2011), Sun * et al. (2013),andZhu et al. (2011) Intradiol ring-cleaving dioxygenase Fungi Tetranychidae (Trombidiformes) ML, G Bajda et al. (2015), Dermauw et al. * (2013),andGrbic et al. (2011) Kynureninase L. grayi bacteria Lepidoptera (Lepidoptera) ML, BI, NJ, G, F Meng et al. (2009), Li et al. (2011)°Sun et al. (2013),andZhu et al. (2011) UDP-glycosyltransferase Bacteria Tetranychidae (Trombidiformes) ML, G Ahn et al. (2014) and Bajda et al. (2015) *

Techniques used to examine each HGT event are listed in the Validation column. The phylogenetic methodologies are abbreviated as ML: Maximum Likelihood analysis of protein sequences, BI: Bayesian Inference, NJ: Neighbor-Joining and MP: Maximum Parsimony. Further analysis include; G: proof of physical incorporation into the arthropod genome and F: enzyme product is functional. An asterisk within column ‘C’ indicates whether a similar gene has been independently horizontally transferred to a phytophagous species within the Fungi, Oomycota, and Nematoda lineage.

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and novel host plants. Here, the horizontally transferred genes are categorized based on how their enzyme products interact with the nutritional and defensive barriers of plants. The cat- egories discussed are: (1) penetration and digestion of plant cell walls, (2) assimilation of plant nutrients, and (3) overcom- ing plant defenses (table 1).

Penetration and Digestion of Plant Cell Walls Various networks of complex composite fibers form the plant cell wall and cuticle and enclose all cells of land plant species. These plant structures are central to the biology of all terres- trial plants as they provide the necessary structural integrity and mechanical support for livingonland.Insomeplantspe- Downloaded from cies, these composite fibers form a thick rigid layer (for in- stance in woody plants), and pose a barrier for arthropods aiming to feed on plant nutrients (Carpita and Gibeaut 1993; Whetten and Sederoff 1995; Heredia 2003; Sorensen et al. 2010). These complex matrices are mainly built from polysaccharides and constitute the largest reservoir of organic http://gbe.oxfordjournals.org/ FIG.3.—Coleopteran phylogenetic tree focusing on the Phytophaga carbon on earth. As all animals, arthropods have an inherently lineage, which harbors the majority of all phytophagous . inadequate battery of enzymes that are able to cleave these Horizontal transfer of genes coding for enzymes that digest plant cell recalcitrant cell wall polysaccharides and access their stored wall components and intracellular carbohydrates and chitinases are de- energy. Some specialized phytophagous arthropods, like picted in blue, green, and orange, respectively. Recent, apparent species- wood-feeding termites, have extensively proliferated a gene specific HGT events are depicted by circles and the name of the recipient family of ancestral animal cellulases to enzymatically cleave species. Dated phylogenetic relationships are scaled in MYA and based on certain cell wall components (Watanabe and Tokuda 2010), different sources (Farrell 1998; Marvaldi et al. 2009). by guest on September 24, 2016 while other arthropods seem to solely rely on microbial sym- bionts in their gut (Breznak 1982). Microorganisms are able to convert the complex fibers of the plant cell wall into simple Independent genomic approaches and in-depth phylogenetic oligo- and monosaccharides by producing unique plant cell analysis provide proof that genes of various microbial GH fam- wall degrading enzymes (PCWDEs). These microbial ilies have been laterally transferred to phytophagan beetle PCWDEs are able to digest the rigid plant cell wall constituents genomes at various time points during their evolution. in the digestive tract and release their stored energy, benefit- Moreover, some laterally acquired genes subsequently dupli- ing both the microorganisms and their arthropod hosts. Most cated and diversified in a lineage-specific manner, while of the PCWDEs belong to various GH families that hydrolyze others were lost and replaced by other, more recently laterally glycosidic bonds either by a single or double displacement acquired GH genes (Shen et al. 2003; Kirsch et al. 2012, 2014; mechanism. GHs are delineated into specific families and sub- Eyun et al. 2014;;Pauchet et al. 2014b; Vega et al. 2015) families through the curated Carbohydrate-Active database of (fig. 3). There is a growing multi-layered body of evidence that enzymes involved in carbohydrate metabolism (Cantarel et al. clearly indicates that these transferred genes code for func- 2009). Although GH families are found across the whole tree tional PCWDE and were of adaptive significance to phytopha- of life, most GH families coding for PCWDEs are restricted to gan beetles. First, transcriptomic and proteomic studies show bacterial and fungal species (Rye and Withers 2000; Gilbert that transcription and translation of these foreign genes is 2010). concentrated in the mid- and hindgut, where the digestion Within the insect orders of the Coleoptera, Phasmatodea, takes place (Pauchet et al. 2009, 2014a; Kirsch et al. 2012, and Hemiptera (fig. 1), studies have indicated that genes 2014; Pauchet and Heckel 2013; Scully et al. 2013). Second, coding for PCWDEs have been laterally transferred to insect in vitro functional expression assays unambiguously prove that genomes enabling the host to degrade the complex cell wall these GH genes continue to code for functionally active en- polysaccharides themselves. Within Coleoptera, the most di- zymes that cleave cell wall constituents (Shen et al. 1996; verse monophyletic clade of herbivorous beetles is the Padilla-Hurtado et al. 2012; Pauchet and Heckel 2013; Phytophaga group (harboring ~80% of all plant feeding bee- Kirsch et al. 2014; Pauchet et al. 2014a). By the horizontal tles) and contains the superfamilies Chrysomeloidea and transfer of new types of GH genes, beetle recipients gained Curculionoidea (Farrell 1998; Marvaldi et al. 2009)(fig. 3). new metabolic capabilities which in turn likely facilitated the

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colonization of novel plant tissues and species. For instance, fungi (fig. 3). Rice weevil, a seed specialist, is however able to cerambycid beetles are wood-feeders and can metabolize demethylate pectin through an independent horizontal trans- xylan, a polysaccharide abundantly present in woody plant mission of bacterial genes of the carbohydrate esterase family tissues, by the enzymes coded by horizontally acquired sub- 8(Shen et al. 1999, 2005; Pauchet et al. 2010a; Kirsch et al. family 2 genes of the extremely diverse GH5 family (Pauchet 2016). These genes code for functional pectin methylesterases et al. 2014a)(fig. 3). Enzyme kinetics also show that post- that remove the methyl-groups of both homogalacturonan transfer gene duplications have led to functional diversifica- and xylogalacturonan. The two independently horizontally ac- tion, potentially further expanding the host plant range of the quired pectin methylesterase and polygalacturonase families beetles (Sugimura et al. 2003; Lee et al. 2005; Pauchet and are shown to act synergistically in the rice weevil’s degradation Heckel 2013; Xia et al. 2013; Kirsch et al. 2014, 2016; Pauchet of plant pectin (Kirsch et al. 2016). Bacterial pectin methyles- et al. 2014a). Such functional diversification is shown by mi- terase genes have been transferred to an ancestral species crobial GH48 genes, which no longer code for PCWDEs with within the Curculionoidea superfamily and could serve a sim- cellobiosidase activity, but have been co-opted by the beetles ilar function in other descendent weevil species (Pauchet et al. to serve as chitinases (Fujita et al. 2006; Sukharnikov et al. 2010a; Evangelista et al. 2015; Kirsch et al. 2016). 2012)(fig. 3).

Seeds of the coffee plant consist of 60% of recalcitrant Downloaded from In addition to Coleoptera, GH28 genes, which code for polymeric carbohydrates of which galactomannan is the major polygalacturonases (fig. 3), were also laterally transferred storage product (Bradbury and Halliday 1990). Within the into the Phasmatodea and Hemiptera lineages and were sub- Hypothenemus genus (Coleoptera: Curculionoidea), H. sequently duplicated within their genomes (Allen and Mertens hampei is a specialist and, in contrast to its close relatives, 2008; Celorio-Mancera et al. 2008; Shelomi et al. 2014)(fig.

can complete a full life cycle when feeding exclusively on http://gbe.oxfordjournals.org/ 1). In contrast to the recurrent and ongoing HGT events in coffee beans. In search for the responsible digestive enzymes, Coleoptera, phylogenetic analysis indicates a single ancient Acuna et al. (2012) discovered a very recent horizontal transfer HGT event within Phasmatodea. Although no GH28 enzyme of a bacterial mannanase gene. The recombinant mannanase has been functionally characterized in this insect lineage yet, enzyme exhibits endo-b-mannanase activity and is able to the genes are also expressed in the gut and show differential metabolize galactomannan extracted from coffee beans, sug- transcript levels along the phasmid digestive tract, strongly gesting that this HGT promoted the transition of the specialist indicative of a role in digestive physiology (Shelomi et al. H. hampei to its current seed diet (fig. 3). 2014). Whereas Phasmatodea and Coleoptera disrupt plant In conclusion, various phytopathogenic and symbiont mi- by guest on September 24, 2016 tissue by chewing, hemipteran insects pierce plant tissue using crobial species provide a source of genetic diversity that allows highly specialized stylet-like mouthparts. Within Hemiptera, arthropod lineages to quickly adapt to recalcitrant plant cell the distribution of laterally acquired polygalacturonase genes wall components. seems to be limited to species of the Mirinae, a subfamily within the large and diverse Miridae family (Allen and Mertens 2008; Celorio-Mancera et al. 2008; Hull et al. Assimilation of Intracellular 2013; Shelomi et al. 2014). These mirid insects digest plant Plant Nutrients material extra-orally by secreting enzymatically active saliva Carbohydrate Metabolism through their stylet into the host (Miles and Taylor 1994). In line with the in plantae digestion of this macerate-and-flush In addition to a polysaccharide-enriched extracellular cell wall, feeding strategy, polygalacturonase genes in mirid plant bugs plants are also characterized by a high intracellular carbohy- are expressed in the salivary glands whereupon the protein drate content (Mattson 1980; Strong et al. 1984). For herbi- products are secreted into the plant (Celorio-Mancera et al. vores, these high intracellular carbohydrate levels represent a 2008). substantial amount of potential energy. Indeed, early studies In addition to their stalks and leaves, plants also accumulate indicate that leaf-feeding caterpillars harvest this energy by a huge amounts of complex cell wall carbohydrates in their dual a-andb-glycosidase activity in their midgut, which seeds (Buckeridge et al. 2000). Many arthropods feed breaks disaccharides down into monosaccharides (Santos exclusively on seeds and show HGT-mediated adaptations and Terra 1986; Sumida et al. 1994). As only microbial organ- to fully utilize the seed’s high carbohydrate content. isms express b-fructofuranosidases (or also called invertases or Homogalacturonan and xylogalacturonan are highly methyl- b-glucosidases) that are able to catalyze b-glucosidase reac- ated polysaccharides that serve as a backbone in the complex tions, it was long postulated that the observed dual activity in pectin network and can be abundantly present in seeds the lepidopteran midgut was a combined product of the (Zandleven et al. 2006). Methylation of the polysaccharide insect and its midgut microflora. The insect host benefits backbone typically inhibits the pectin cleaving activity of poly- from its microflora, as a-andb-glycosidases only hydrolyze galacturonase enzymes, including those that are produced by terminal a-andb-linked glucosyl residues, respectively, and weevils (Coleoptera: Curculionoidea) after an HGT event from differ in substrate specificities (Terra and Ferreira 1994).

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However, more recent studies started to indicate that these 2011). Arthropod herbivores again have taken advantage of digestive enzymes might be expressed by the insects them- the microbial metabolic richness and harbor horizontally trans- selves and not by associated symbionts (Carneiro et al. 2004; ferred genes that code for enzymes with key roles in de novo Pauchet et al. 2008). The study of Daimon et al. (2008) shows nutrient synthesis. Both the functional replacement of pre- that a Bombyx mori gene of the GH32 family codes for a existing metabolic traits as well as the acquisition of comple- functional b-fructofuranosidase and claims that this is ac- tely new ones by HGT have occurred in phytophagous arthro- quired by an HGT from a bacterial donor. Further phylogenetic pod lineages (Meng et al. 2009; Moran and Jarvik 2010; Grbic analysis and genome mining shows that close homologues of et al. 2011; Sun et al. 2013; Luan et al. 2015). For instance, the B. mori GH32 gene are present in all lepidopteran ge- carotenoid biosynthesis genes detected in dipteran, hemip- nomes sequenced so far, suggestive of a single ancient HGT teran, and tetranychid genomes, but nowhere else in the about 145-200 MYA (Li et al. 2011; Zhu et al. 2011; Sun et al. animal kingdom, all have a high similarity to fungal homo- 2013). In addition, current comparative genomic studies logues, leading multiple studies to conclude that these were across the Arthropoda also uncovered the presence of b-fruc- laterally acquired from fungal donors. These genes have been tofuranosidase genes in the genomes of beetles belonging to proven to still code for functional enzymes and likely offer phytophagous arthropods the unique ability to endogenously

the Curculionoidea and Buprestoidea superfamilies, the dip- Downloaded from teran Mayetolia destructor and in the chelicerate spider mite T. produce carotenoids, which are conjugated isoprenoid mole- urticae, suggestive of multiple, independent HGT events cules (Moran and Jarvik 2010; Grbic et al. 2011; Altincicek (Grbic et al. 2011; Keeling et al. 2013; Sun et al. 2013; et al. 2012; Novakova and Moran 2012; Bryon et al. 2013; Pedezzi et al. 2014; Zhao et al. 2014, 2015)(figs. 1 and 3 Cobbs et al. 2013). and table 1). The alternative evolutionary scenario explaining Relative to other plant tissues, phloem, which translocates http://gbe.oxfordjournals.org/ the presence of b-fructofuranosidase genes in the genomes of photosynthate, is especially low in essential amino acids and these phytophagous arthropods and their absence in all other vitamins (Sandstrom and Pettersson 1994; Sandstrom and sequenced arthropod genomes so far is that a gene copy was Moran 1999). Hemipteran insects are nonetheless able to present in an arthropod ancestor and subsequently lost in all feed exclusively on phloem sap. At first glance, HGT would individual lineages across the whole arthropod phylogenetic not seem to be required, as hemipterans supplement their tree (fig. 1).Fornow,thisisafarlessparsimoniousscenario phloem diet with nutrients by engaging in intimate symbiotic due to the extremely high prevalence of gene loss that would associations with bacteria. Hemipterans form an organ, the bacteriome, where bacteria are sequestered into specialized be required. Moreover, phylogenetic analysis strongly sug- by guest on September 24, 2016 gests independent horizontal transfers of the b-fructofurano- host cells called bacteriocytes (Buchner 1965). This symbiosis sidase genes from different bacterial donor species to the benefits both insect and endosymbiont, since the bacteria re- diverse phytophagous lineages (Keeling et al. 2013; Pedezzi ceive a steady flow of nutrients and in return provide the sap- et al. 2014; Zhao et al. 2014). As within Lepidoptera, the feeding hemipteran host with essential amino acids and vita- transferred gene into the Curculionoidea superfamily still mins. After the original bacterial inoculation of the bacteriome codes for a functional b-fructofuranosidase (Pedezzi et al. organ, these symbiotic bacteria go through extreme popula- 2014). tion bottlenecking, facilitating the fixation of non-functional In all sequenced lepidopteran genomes, horizontally trans- mutations by genetic drift and resulting in progressive geno- ferred genes of a bacterial origin have been identified that mic decay. As the bacterial genome deteriorates, the symbi- code for enzymes classified as GHs of the 31 family. onts become more and more dependent on the metabolism Although these genes are not yet functionally characterized, of their insect hosts, mirroring the evolution of organelles GH31 genes often code for enzymes that cleave oligosaccha- (Mccutcheon and Moran 2012). Gene losses in vitamin, rides (Cantarel et al. 2009; Sun et al. 2013; Wheeler et al. amino acid and other synthetic pathways unique to bacteria 2013). have been observed, endangering the persistence of the mu- These studies suggest that horizontally transferred genes tualistic symbiosis as the insect host does not produce the from various sources offer selective advantages to phytopha- necessary battery of enzymes. By sequencing the genomes gous arthropods by enabling them to fully harvest the carbo- of different hemipteran insects, a convergent evolutionary hydrate-rich compositions of plant tissue (table 1). trend emerged in that independent HGT events from other, free-living bacteria to the insect genome counteract the ge- nomic deterioration of unique bacterial pathways within the Amino Acid, Vitamin, and Carotenoid Metabolism endosymbionts (Husnik et al. 2013; Sloan et al. 2014; Luan Compared with animals, bacteria and fungi exhibit an ex- et al. 2015). For instance, both the citrus mealybug and silver- tremely high diversity of biosynthetic metabolic networks. leaf whitefly possess multiple horizontally acquired genes that This rich enzymatic repertoire enables microorganisms to function within the microbial lysine synthesis pathway (Luan uniquely synthesize certain compounds, some of which have et al. 2015). Genome analysis of various hemipteran hosts and been defined as vitamins (Karlin et al. 2001; LeBlanc et al. their symbionts revealed that several gene losses within the

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bacterial biosynthesis pathways of the vitamins biotin and ri- two arthropod lineages co-opted this bacterial gene to serve in boflavin have been compensated by multiple, independent their xenobiotic metabolism with significant ecological HGT events to the host (table 1)(Husnik et al. 2013; Sloan consequences. et al. 2014; Luan et al. 2015). The transcription of these for- In addition to a CAS gene, spider mites also laterally ac- eign genes is often concentrated in the bacteriocytes where quired a gene that codes for a functional cyanase enzyme. As the enzyme products can readily interact with the intermedi- cyanase metabolizes noxious cyanate, a common oxidation ate substrates within the bacterial synthetic pathways (Husnik product of cyanide, into nontoxic products, it may represent et al. 2013; Sloan et al. 2014; Luan et al. 2015). a second, alternative route of cyanide detoxification in phy- tophagous spider mites. Indeed, cyanase gene-expression was Overcoming Plant Defenses induced in mites feeding on cyanogenic bean, compared to an acyanogenic bean cultivar. However, transcription analysis In response to the selection pressure of herbivore attacks, across a wider range of host plants led Wybouw et al. plants have developed numerous anti-herbivore physical and (2012) to conclude that it may also serve other biological func- chemical defenses. Plant toxins and their mode of action vary tions (such as regulation of amino acid metabolism). widely across the plant kingdom (Whittaker and Feeny 1971; Aromatic ring structures are commonly found in plant Downloaded from Howe and Jander 2008), and HGT events have been impli- toxins and give these compounds an exceptionally high stabil- cated in arthropod adaptations to some of them. ity due to their resonance structure. Phytopathogenic fungi Mulberry plants defend themselves by accumulating alka- nevertheless metabolize complex catecholic metabolites, loid compounds in their foliar latex layer. These alkaloids deter such as procyanidins, by secreting intradiol ring-cleaving herbivores from feeding by strongly inhibiting their a-glycosi- dioxygenases. This family of dioxygenases, restricted to http://gbe.oxfordjournals.org/ dase activity. Functional characterization of the B. mori b-fruc- microorganisms, catalyze the oxygenolytic fission of aromatic tofuranosidase, coded by the horizontally transferred GH32 structures between adjacent hydroxyl groups (Vaillancourt gene, showed that the enzyme is not only active but also et al. 2006; Roopesh et al. 2010, 2012; Yang et al. 2012). insensitive to these inhibitory alkaloids. Therefore, Daimon An intradiol ring-cleaving dioxygenase has been horizontally et al. (2008) claimed that after HGT to an ancestor and sub- transferred into the plant feeding Tetranychidae mite family sequent natural selection, B. mori was able to specialize on with secreted fungal enzymes as its closest homologues. Here, mulberry plants by co-opting this carbohydrate metabolizing the dioxygenase gene duplicated and currently forms multi- enzyme in its defenses. gene families in descendent mite species (for instance, the T. by guest on September 24, 2016 Cyanogenic plants release poisonous cyanide from non- urticae genome harbors 17 intradiol dioxygenase genes). toxic precursor compounds upon herbivore attack Previous studies uncovered a high transcriptional response of (Zagrobelny et al. 2008). Like plants, bacteria are also able this unique gene family to various chemical stresses, including to biosynthesize cyanide and both prevent auto-toxicity by host plants and acaricides (Grbic et al. 2011; Dermauw et al. producing a CAS enzyme. CAS efficiently detoxifies cyanide 2013; Bajda et al. 2015; Van Leeuwen and Dermauw 2016). by incorporating it into cysteine, hereby releasing the amino Although this dioxygenase gene family awaits functional char- acid derivative b-cyanoalanine (Miller and Conn 1980; Ebbs acterization, current data strongly suggest that mites use 2004). In contrast, animals have less efficient cyanide detoxi- these laterally acquired genes in their detoxification pathways. fication pathways, making cyanide an effective allelochemical As well as detoxifying, some arthropod herbivores also sup- (Beesley et al. 1985; Zagrobelny et al. 2008). In-depth phylo- press toxin production to avoid the negative effects on their genetic analysis from different studies indicates that at differ- reproductive performance. Such manipulation of plant physi- ent times in arthropod evolution, spider mites and Lepidoptera ology by arthropods (and other herbivores) is achieved by se- independently acquired genes related to characterized CAS creting salivary compounds into the plant where these genes from a common bacterial clade often associated with interfere with plant pathways (Kant et al. 2015; Zhao et al. the phyllosphere. Functional characterization of both mite and 2015; Villarroel et al. 2016). Aromatic allelochemicals (includ- lepidopteran recombinant CAS enzymes shows that they con- ing flavonoids) are produced by enzymes of the conserved vert toxic cyanide rapidly into b-cyanoalanine (Wybouw et al. shikimate pathway, restricted to plants and bacteria 2014; Van Ohlen et al. 2016). Furthermore, it is shown in (Herrmann 1995). Specifically, the aromatic toxins are derived caterpillars that CAS activity is widespread and inducible from chorismate, the end product of the shikimate pathway upon exposure to dietary cyanide (Witthohn and Naumann, (Strack 1997). CM is a key branch-point enzyme that converts 1987; Meyers and Ahmad 1991; Stauber et al. 2012). By en- chorismate to prephenate (Romero et al. 1995). In plant par- dogenously producing this cyanide detoxifying enzyme, some asitic nematodes, it has been proposed that by horizontal Lepidoptera could not only colonize a whole new range of transfer of a CM gene, nematodes are able to modulate the host plants, but also develop their own cyanogenic defenses plant shikimate pathway to their own benefit (Lambertetal. to deter predators (Witthohn and Naumann 1987; Zagrobelny 1999; Vanholme et al. 2009; Haegeman et al. 2011). The et al. 2008). These studies provide strong evidence that these discovery of a horizontally transferred CM gene in multiple

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hemipteran lineages now raises the question whether it serves bacterial donor, the mobile genetic element needs to be ex- a similar function there (Husnik et al. 2013; Luan et al. 2015) pressed by a functionally appropriate promoter and adjusted (table 1). to the eukaryotic transcription machinery (polyadenylation, These examples show that arthropods have evolved various codon compositions, and binding site modifications). Last, in counter adaptations to their host plants’ defenses by hijacking multicellular eukaryotes, a new laterally acquired genetic ele- pre-evolved genes from bacteria and fungi, some of which ment can only be transmitted to the following generation if it share the same metabolic pathways as plants. is incorporated within the isolated germ cell line. Arthropods have widespread and intimate relationships with bacterial Parallel Roles for HGT in Other communities which consist of free-living bacterial species and/or of symbiotic bacteria that permanently reside within Eukaryotic Linages certain arthropod organs (Buchner 1965; Hotopp et al. 2007; Moreover, a role of HGT in the evolutionary transition towards Hotopp 2011; Li et al. 2011). Even the reproductive tissues of exploiting plants, whether by herbivory or a phytopathogenic arthropods are commonly infected with intracellular endosym- strategy, has also been suggested in three other eukaryotic biotic bacteria. Some endosymbionts are extremely closely as- lineages, namely Fungi, Oomycota (Heterokontophyta) and sociated with germ line tissues as they are able to interfere Downloaded from the animal phylum of Nematoda. The genomic innovations with the reproductive processes of their arthropod hosts in due to HGT have shaped the penetration, assimilation and order to increase their vertical transmission to the next gener- detoxification pathways of plant tissue independently and in ation (Stouthamer et al. 1999; Hotopp et al. 2007; Hotopp, parallel within these phylogenetically diverse plant parasites 2011). Although the barriers of HGT to a eukaryote are high, (Danchin et al. 2010; Haegeman et al. 2011; Soanes and the close proximity of dense and complex bacterial popula- http://gbe.oxfordjournals.org/ Richards 2014). Comparing these studies with the data re- tions around and within arthropods at least facilitates HGT to viewed here, it is apparent that a significant number of the germ cell line. genes coding for enzymes with identical catalytic properties In prokaryotes, HGT is known to operate through three were horizontally transferred to these highly divergent line- mechanisms, namely (1) transformation—the direct uptake ages where they play similar roles in the herbivorous lifestyle of exogenous DNA, (2) conjugation—the plasmid-mediated (table 1). For instance, laterally acquired PCWDEs and b-fruc- uptake of foreign DNA through cell-to-cell contact, and (3) tofuranosidases are also found in a wide range of plant par- transduction—the virus-mediated uptake of foreign DNA asitic nematodes and are responsible for the digestion of (fig. 2A). Studies have found that some laterally transferred by guest on September 24, 2016 recalcitrant plant cell wall components and host-derived su- genes in animal recipients are linked to genomic regions en- crose, respectively (Danchin et al. 2010, 2016). Moreover, riched in TEs (Acuna et al. 2012; Paganini et al. 2012; Flot et al. horizontally transferred genes have a tendency to duplicate 2013; Pauchet and Heckel 2013; Gasmi et al. 2015). TEs are and form novel multi-gene families across the four lineages, mobile and can jump within and between genomes. Other strongly indicative of functional diversification (Danchin et al. genes close to these TEs could potentially hitchhike on such a 2010; Dermauw et al. 2013; Ahn et al. 2014; Kirsch et al. transposition event between close physical interacting organ- 2014). isms (through endosymbiosis, husbandry, parasitism, preda- The strong parallel role of HGT in the evolution of plant torism or other forms of contact). Moreover, studies indicate exploitation across different eukaryotic linages indicates that that viruses can act as a shuttle for TE-mediated HGT (Liu et al. the genomes of non-related microorganisms already adapted 2010; Gilbert et al. 2014; Gasmi et al. 2015). For instance, to living on and from plants provide a great adaptive potential parasitoid wasps inject bracoviral particles into their lepidop- for eukaryotes trying to colonize the same niche. teran hosts to aid in the development of their offspring. Genome analysis revealed that wasp genes have been stably Potential Mechanisms of HGT to incorporated into lepidopteran species through the bracoviral integration mechanism (Gasmi et al. 2015). As viruses can act Arthropod Herbivores as gene transfer agents, the donor and recipient species do Because HGT to a eukaryotic recipient has only been detected not necessarily have to be in direct physical contact, further after the fact, the exact mechanisms of the transfer remain increasing the potential source of alien genetic information elusive. HGT must be a multi-step process whereby a genetic (Houck et al. 1991; Dimmock et al. 2007; Liu et al. 2010; element is excised from a donor genome, transmitted and Gilbert et al. 2014; Gasmi et al. 2015). Extracellular vesicles, introduced into a reproductively isolated recipient genome. such as exosomes, could also be a potential route of gene Multiple facets of eukaryotic biology seem to lower the likeli- transfer into eukaryotic species. These vesicles function in hood of successfully completing this multi-step process. First, intercellular communication and are produced by organisms before genetic information can be integrated and expressed in throughout the domains of life. They contain various com- a eukaryotic genome, it first has to pass through the selective pounds, including DNA and RNA molecules. Notably, within double membrane of the nucleus. Second, if it concerns a bacteria, genetic information is known to be transferred not

Genome Biol. Evol. 8(6):1785–1801. doi:10.1093/gbe/evw119 Advance Access publication June 15, 2016 1797 Wybouw et al. GBE

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